Coordinated microRNA and messenger RNA expression profiles for understanding sexual dimorphism of gonads and the potential roles of microRNA in the steroidogenesis pathway in Nile tilapia (Oreochromis niloticus)

Wang, Weiwei; Liu, Wenzhong; Liu, Qing; Li, Baojun; An, Lifeng; Hao, Ruirong; Zhao, Jianmin; Liu, Shaozhen; Song, Jing

doi:10.1016/j.theriogenology.2015.11.006

Cited by 37 publications

(26 citation statements)

References 53 publications

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“…Two miRNAs in cluster V, miR-25 and miR-181a, were abundant in zebrafish spermatozoa [ 45 ], while miR-2188 is expressed in halibut gonads but has not been associated with testis maturation yet [ 30 ]. miR-20a , a sexually dimorphic miRNA, is a possible target of DMRT-1 in the testis of Nile tilapia [ 53 ]. In addition to miRNAs that previous work has linked to testis maturation, we found miRNAs in cluster V that have not been reported so far as linked to testis maturation, such as miR-731 , miR-8157 and the novel predicted n2 .…”

Section: Resultsmentioning

confidence: 99%

Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon

et al. 2017

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BackgroundOur understanding of the molecular mechanisms implementing pubertal maturation of the testis in vertebrates is incomplete. This topic is relevant in Atlantic salmon aquaculture, since precocious male puberty negatively impacts animal welfare and growth. We hypothesize that certain miRNAs modulate mRNAs relevant for the initiation of puberty. To explore which miRNAs regulate mRNAs during initiation of puberty in salmon, we performed an integrated transcriptome analysis (miRNA and mRNA-seq) of salmon testis at three stages of development: an immature, long-term quiescent stage, a prepubertal stage just before, and a pubertal stage just after the onset of single cell proliferation activity in the testis.ResultsDifferentially expressed miRNAs clustered into 5 distinct expression profiles related to the immature, prepubertal and pubertal salmon testis. Potential mRNA targets of these miRNAs were predicted with miRmap and filtered for mRNAs displaying negatively correlated expression patterns. In summary, this analysis revealed miRNAs previously known to be regulated in immature vertebrate testis (miR-101, miR-137, miR-92b, miR-18a, miR-20a), but also miRNAs first reported here as regulated in the testis (miR-new289, miR-30c, miR-724, miR-26b, miR-new271, miR-217, miR-216a, miR-135a, miR-new194 and the novel predicted n268). By KEGG enrichment analysis, progesterone signaling and cell cycle pathway genes were found regulated by these differentially expressed miRNAs. During the transition into puberty we found differential expression of miRNAs previously associated (let7a/b/c), or newly associated (miR-15c, miR-2184, miR-145 and the novel predicted n7a and b) with this stage. KEGG enrichment analysis revealed that mRNAs of the Wnt, Hedgehog and Apelin signaling pathways were potential regulated targets during the transition into puberty. Likewise, several regulated miRNAs in the pubertal stage had earlier been associated (miR-20a, miR-25, miR-181a, miR-202, let7c/d/a, miR-125b, miR-222a/b, miR-190a) or have now been found connected (miR-2188, miR-144, miR-731, miR-8157 and the novel n2) to the initiation of puberty.ConclusionsThis study has - for the first time - linked testis maturation to specific miRNAs and their inversely correlated expressed targets in Atlantic salmon. The study indicates a broad functional conservation of already known miRNAs and associated pathways involved in the transition into puberty in vertebrates. The analysis also reveals miRNAs not previously associated with testis tissue or its maturation, which calls for further functional studies in the testis.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4205-5) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon

et al. 2017

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“…In fish, the miRNA distribution in organs of the reproductive axis (brain, pituitary and gonad) has recently been reported in mature stages of the Atlantic halibut [ 44 ], yellow catfish [ 41 ], and Nile tilapia [ 17 , 43 ]. However, to date there is little data on miRNAs that have a possible role in early sex differentiation, especially in fish gonads.…”

Section: Discussionmentioning

confidence: 99%

“…As in tilapia, miR-499 is also a dominant miRNA in swine, indicating its involvement in testicular development [ 71 ]. miR-9 and miR-192 are also upregulated in tilapia ovary, while miR-27d, miR-29b, miR-92b, miR-144-5p and miR-455 show the same pattern of greater expression in testes at later stage [ 43 ], suggesting they might play crucial roles in tilapia sex differentiation. However, the function of most other sex-biased miRNAs was previously unknown.…”

Section: Discussionmentioning

confidence: 99%

“…miR-141 and miR-429 have crucial functions in yellow catfish testis development and spermatogenesis [ 41 ]. Different expression pattern of miRNAs is observed between the embryos of females and males [ 42 ], as well as the ovaries and testes in tilapia gonads at later stages [ 17 , 43 ], indicating their regulatory roles during fish reproduction. let-7a, miR-143, and miR-202 are upregulated to induce testes differentiation in halibut [ 44 ].…”

Section: Introductionmentioning

confidence: 99%

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Integrated analysis of miRNA and mRNA expression profiles in tilapia gonads at an early stage of sex differentiation

et al. 2016

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BackgroundMicroRNAs (miRNAs) represent a second regulatory network that has important effects on gene expression and protein translation during biological process. However, the possible role of miRNAs in the early stages of fish sex differentiation is not well understood. In this study, we carried an integrated analysis of miRNA and mRNA expression profiles to explore their possibly regulatory patterns at the critical stage of sex differentiation in tilapia.ResultsWe identified 279 pre-miRNA genes in tilapia genome, which were highly conserved in other fish species. Based on small RNA library sequencing, we identified 635 mature miRNAs in tilapia gonads, in which 62 and 49 miRNAs showed higher expression in XX and XY gonads, respectively. The predicted targets of these sex-biased miRNAs (e.g., miR-9, miR-21, miR-30a, miR-96, miR-200b, miR-212 and miR-7977) included genes encoding key enzymes in steroidogenic pathways (Cyp11a1, Hsd3b, Cyp19a1a, Hsd11b) and key molecules involved in vertebrate sex differentiation (Foxl2, Amh, Star1, Sf1, Dmrt1, and Gsdf). These genes also showed sex-biased expression in tilapia gonads at 5 dah. Some miRNAs (e.g., miR-96 and miR-737) targeted multiple genes involved in steroid synthesis, suggesting a complex miRNA regulatory network during early sex differentiation in this fish.ConclusionsThe sequence and expression patterns of most miRNAs in tilapia are conserved in fishes, indicating the basic functions of vertebrate miRNAs might share a common evolutionary origin. This comprehensive analysis of miRNA and mRNA at the early stage of molecular sex differentiation in tilapia XX and XY gonads lead to the discovery of differentially expressed miRNAs and their putative targets, which will facilitate studies of the regulatory network of molecular sex determination and differentiation in fishes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2636-z) contains supplementary material, which is available to authorized users.

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“…Many sex-related genes that have been identified in mammals and birds also exist in TSD turtles, and previous studies have found significant differences in gene expression in the adult gonads of the Reeves' pond turtle (Mauremys reevesii) (Xiong et al, 2019). Increasing evidence indicates that microRNAs (miRNAs) may be involved in this dynamic process (Dai and Ahmed, 2014;Wang et al, 2016). However, it is not clear how the regulatory network comprising miRNAs changes the expression levels of these genes.…”

Section: Introductionmentioning

confidence: 99%

Comparison of Adult Testis and Ovary MicroRNA Expression Profiles in Reeves’ Pond Turtles (Mauremys reevesii) With Temperature-Dependent Sex Determination

et al. 2020

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Coordinated microRNA and messenger RNA expression profiles for understanding sexual dimorphism of gonads and the potential roles of microRNA in the steroidogenesis pathway in Nile tilapia (Oreochromis niloticus)

Cited by 37 publications

References 53 publications

Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon

Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon

Integrated analysis of miRNA and mRNA expression profiles in tilapia gonads at an early stage of sex differentiation

Comparison of Adult Testis and Ovary MicroRNA Expression Profiles in Reeves’ Pond Turtles (Mauremys reevesii) With Temperature-Dependent Sex Determination

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